On the Structural Continuities of the Transverse Tubular System of Rabbit and Human Myocardial Cells

Abstract

An electron microscopic study of rabbit and human myocardium provides further evidence of the existence of two distinct components of the sarcoplasmic reticulum. A thin-walled tubular system (termed longitudinal system) is arranged in anastomosing channels sursurrounding each sarcomere and has transverse and possibly also longitudinal connections with the tubules of adjacent sarcomeres. A thick-walled tubular system traverses the myofiber transversely at the level of the Z lines of the myofibrils. The structure of these tubules very closely resembles that of deep sarcolemmal invaginations. Indeed, the membranes of the tubules appear to be continuous with the sarcolemma in favorable sections so that there seems to be an extension of the cell membrane and extracellular fluid to all depths of the myocardial fiber. Certain physiologic data which support this concept are discussed. The calculations of A. V. Hill comparing the kinetics of diffusion and the time-distance relationships between excitation and activation in frog sartorius muscle are reconsidered for cardiac muscle.After Bennett and Porter's first electron microscopic observations of the sarcoplasmic reticulum in the breast muscle of the domestic fowl (I), Porter and Palade presented detailed descriptions of this subcellular structure in different types of striated muscle (2). These findings provided a structural basis for consideration of the mechanisms of excitation-contraction coupling in muscle.Using a micropipette electrode to achieve local depolarization of the cell membrane, Huxley and Taylor (3) demonstrated transverse, two-dimensional conduction of excitation toward the central axis of an isolated intact fiber of frog striated muscle. The geometry of excitation and spread indicated very strongly that conduction inward took place along some structure in the plane of the Z lines of the myofibrils lying in register with one another. This conclusion conformed with an earlier prediction by A. V. Hill (4), based on consideration of the kinetics of diffusion and the time-distance relationships between excitation and activation in frog sartorius muscle. Hill proposed that, while excitation undoubtedly occurred at the cell surface, diffusion was far too slow a means of bearing the impulse into the interior of the fiber. He concluded that a process, not a substance, must carry the excitation inward.The electron microscopic observations of Porter and Palade (2) suggested the possible role of transversely oriented elements of the sarcoplasmic reticulum in excitation-contraction coupling.

Regulation of Cardiac Muscle Contractility

“…Variations in the amount of calcium released during excitation-contraction coupling would be expected to modify myocardial contractility and shortening velocity if the heart's contraction is normally limited by the availability of intracellular calcium. The latter view is supported by the finding that the cardiac sarcoplasmic reticulum, which is presumed to contain this calcium, is less extensive than that of skeletal muscle (48)(49)(50). Because the sensitivities of cardiac and skeletal actomyosins to changing levels of Ca ++ are similar (42,43,51), these anatomical findings indicate that the heart's sarcoplasmic reticulum may normally contain less calcium than is needed to activate the cardiac actomyosin fully.…”

Heart Muscle Antibodies in Rheumatic Fever and Other Diseases*

“…Recent electron microscopy studies (11,12) have demonstrated that the sarcolemma is a complex structure that consists of as many as four separate layers not only surrounding the myofiber but also forming an extensive connecting system around and between the individual myofibrils. The subsarcolemmal and intermyofibrillar areas also contain sarcoplasmic components and mitochondria.…”

Sarcolemmal Invaginations Constituting the T System in Fish Muscle Fibers

“…In heart muscle, for example, invaginations of the sarcolemma have been demonstrated in several cases to penetrate into the fiber (11,36,55,56). Since these start at the periphery of the fiber at the Z line level and run at this level across the fiber for at least a few microns, their homology with the T system is evident.…”